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Resource Partitioning Among Brachiopods and Bivalves at Ancient Hydrocarbon Seeps: a Hypothesis

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Resource Partitioning Among Brachiopods and Bivalves at Ancient Hydrocarbon Seeps: a Hypothesis RESEARCH ARTICLE Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis 1 2 Steffen Kiel , JoÈ rn PeckmannID * 1 Swedish Museum of Natural History, Department of Palaeobiology, Stockholm, Sweden, 2 UniversitaÈt Hamburg, Center for Earth System Research and Sustainability, Institute for Geology, Hamburg, Germany * [email protected] a1111111111 a1111111111 a1111111111 Abstract a1111111111 a1111111111 Brachiopods were thought to have dominated deep-sea hydrothermal vents and hydrocar- bon seeps for most of the Paleozoic and Mesozoic, and were believed to have been outcom- peted and replaced by chemosymbiotic bivalves during the Late Cretaceous. But recent findings of bivalve-rich seep deposits of Paleozoic and Mesozoic age have questioned this OPEN ACCESS paradigm. By tabulating the generic diversity of the dominant brachiopod and bivalve Citation: Kiel S, Peckmann J (2019) Resource clades±dimerelloid brachiopods and chemosymbiotic bivalves±from hydrocarbon seeps partitioning among brachiopods and bivalves at through the Phanerozoic, we show that their evolutionary trajectories are largely unrelated ancient hydrocarbon seeps: A hypothesis. PLoS to one another, indicating that they have not been competing for the same resources. We ONE 14(9): e0221887. https://doi.org/10.1371/ journal.pone.0221887 hypothesize that the dimerelloid brachiopods generally preferred seeps with abundant hydrocarbons in the bottom waters above the seep, such as oil seeps or methane seeps Editor: JuÈrgen Kriwet, University of Vienna, AUSTRIA with diffusive seepage, whereas seeps with strong, advective fluid flow and hence abundant hydrogen sulfide were less favorable for them. At methane seeps typified by diffusive seep- Received: June 13, 2019 age and oil seeps, oxidation of hydrocarbons in the bottom water by chemotrophic bacteria Accepted: August 16, 2019 enhances the growth of bacterioplankton, on which the brachiopods could have filter fed. Published: September 5, 2019 Whereas chemosymbiotic bivalves mostly relied on sulfide-oxidizing symbionts for nutrition, Peer Review History: PLOS recognizes the for the brachiopods aerobic bacterial oxidation of methane and other hydrocarbons played a benefits of transparency in the peer review more prominent role. The availability of geofuels (i.e. the reduced chemical compounds process; therefore, we enable the publication of used in chemosynthesis such as hydrogen sulfide, methane, and other hydrocarbons) at all of the content of peer review and author responses alongside final, published articles. The seeps is mostly governed by fluid flow rates, geological setting, and marine sulfate concen- editorial history of this article is available here: trations. Thus rather than competition, we suggest that geofuel type and availability con- https://doi.org/10.1371/journal.pone.0221887 trolled the distribution of brachiopods and bivalves at hydrocarbon seeps through the Copyright: © 2019 Kiel, Peckmann. This is an open Phanerozoic. access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are Introduction in the paper. The idea of bivalves replacing brachiopods as the dominant benthic filter feeders over the Funding: The authors received no specific funding course of the Phanerozoic is one of the oldest macroevolutionary patterns discussed in paleon- for this work. tology [1±3]. Originally observed in the rich fossil record of shallow marine environments, a PLOS ONE | https://doi.org/10.1371/journal.pone.0221887 September 5, 2019 1 / 22 Paleoecology of seep-dwelling brachiopods and bivalves Competing interests: The authors have declared similar pattern was also seen at deep-sea hydrothermal vents and hydrocarbon seeps [4]. These that no competing interests exist. ecosystems differ radically from all others in being based on chemosynthetic primary produc- tion rather than photosynthesis [5]. The evolution of the chemosynthesis-based faunal com- munities may therefore be buffered from mass extinctions and other disruptions of photosynthesis-based food chains [6±8] and may instead be driven by events affecting the dis- charge of the reduced chemicals (referred to as geofuels hereafter) that fuel the chemosynthe- sis-based food chain [9]. The animals that dominate chemosynthesis-based ecosystems show extensive physiological adaptations, commonly involving a symbiosis with chemotrophic bac- teria, resulting in faunal communities with a low diversity but high abundance of highly spe- cialized animals [10, 11]. A first compilation of Phanerozoic vent and seep sites with brachiopods and/or bivalves indicated a pattern of a Paleozoic to middle Mesozoic dominance of brachiopods in these eco- systems, and the chemosymbiotic bivalves became dominant from the Late Cretaceous onward [4]. Subsequent research confirmed a number of Paleozoic and early Mesozoic seep deposits dominated by brachiopods, including Septatrypa in the Silurian [12], Dzieduszyckia in the Devonian [13], Ibergirhynchia in the Carboniferous [14], Halorella in the Triassic [15], and Sulcirostra and Anarhynchia in the Jurassic [16±18], supporting this hypothesis. However, also discovered were seep deposits at which inferred chemosymbiotic bivalves were a major faunal element, including the modiomorphid genus Ataviaconcha at Silurian and Devonian sites in Morocco [19, 20] and kalenterid and anomalodesmatan genera at Triassic sites in Turkey [21, 22]. These findings challenge the claim of predominantly brachiopod-dominated pre-Creta- ceous vents and seeps, and raise the questions why some sites were dominated by brachiopods and others by bivalves. A further complication in this context is that the feeding strategy (or strategies) of vent and seep-inhabiting brachiopods is essentially unknown. The large size of certain species and bra- chiopod dominance at some sites may intuitively suggest that they were chemosymbiotic [18, 23, 24]. However, brachiopods are virtually absent from extant vents and seeps, and the few known examples are filter feeder that take advantage of the hard substrate provided by authi- genic carbonates exposed at some seeps [25]. Furthermore, the general brachiopod bauplan lacks certain features, such as gills and a closed cardio-vascular system, which are important for hosting chemosymbionts in bivalves or tube worms [26, 27] and make brachiopods ill- suited for coping with the toxicity of hydrogen sulfide. Furthermore, the brachiopods that formed mass occurrences at ancient seeps are not drawn randomly from the brachiopod tree of life but instead belong, with one exception, to a single clade: the Dimerelloidea [28]. The one exception is the genus Septatrypa from a Silurian seep deposit in Morocco [12], which belongs to a different rhynchonellate order than the dimerelloids. Because insights into the feeding strategy of seep-dominating brachiopods are only available for the dimerelloids (see below), our study focuses exclusively on members of this clade. One intriguing feature of many seep deposits dominated by dimerelloids is the sheer abundance of the brachiopods, which by far exceeds the abundance of chemosymbiotic bivalves at fossil seep deposits ([13, 15, 17, 29], own observations). Here we present the hypothesis that dimerelloid brachiopods and chemosymbiotic bivalves coexisted at hydrocarbon seeps during the Paleozoic and Mesozoic by partitioning the locally available geofuels. We propose that the presence, absence, or relative abundance of each clade at a given site was largely controlled by the chemical composition of the seep fluids (the pro- portions of sulfide, methane, and/or oil), which in turn was influenced by seepage intensity and perhaps seawater sulfate concentrations. Our hypothesis is based on (i) a tabulation of the diversity of the ecologically dominant bivalve and brachiopod genera at seeps through the Phanerozoic; (ii) recent improvements in geochemically assessing the composition of fluids PLOS ONE | https://doi.org/10.1371/journal.pone.0221887 September 5, 2019 2 / 22 Paleoecology of seep-dwelling brachiopods and bivalves and the intensity of fluid flow at ancient seeps; and (iii) a set of derivations and assumptions on the paleoecology of the dominant brachiopod and bivalve clades at ancient hydrocarbon seeps. Approach Compilation of generic diversity of bivalves and brachiopods Modern seep communities are characterized by the low diversity but high abundance of a few taxa that are able to take advantage of the unique food resources at seeps [5, 30]. Thus our compilation of brachiopod and bivalve diversity at seeps includes only the ecologically domi- nant clades instead of the full range of genera known from fossil seep deposits to avoid the results being blurred by chance occurrences or by local taxa fortuitously taking advantage of the abundance of food at a seep site (known as `vagrants' or `background taxa', cf. [31] Sibuet and Olu, 1998). Among bivalves, only chemosymbiotic or in the case of extinct taxa, inferred chemosymbiotic taxa, were included. Although chemosymbiotic bivalves may occasionally be rare, in general they dominate seep deposits numerically (cf. [9] Kiel, 2015; [32] Campbell, 2006). Among brachiopods, only dimerelloid genera reported from geochemically confirmed seep deposits are included because (i) with a single exception (see
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